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OPEN Tracking the rising risk of and rays in the Northeast and Rachel H. L. Walls* & Nicholas K. Dulvy

The loss of is increasingly well understood on land, but trajectories of extinction risk remain largely unknown in the ocean. We present Indices (RLIs) to track the extinction risk of 119 Northeast Atlantic and 72 Mediterranean and ray primarily threatened by overfshing. We combine two IUCN workshop assessments from 2003/2005 and 2015 with a retrospective backcast assessment for 1980. We incorporate predicted categorisations for Data Defcient species from our previously published research. The percentage of rose from 1980 to 2015 from 29 to 41% (Northeast Atlantic) and 47 to 65% (Mediterranean Sea). There are as many threatened sharks and rays in Europe as there are threatened birds, but the threat level is nearly six times greater by percentage (41%, n = 56 of 136 vs. 7%, n = 56 of 792). The Northeast Atlantic RLI declined by 8% from 1980 to 2015, while the higher-risk Mediterranean RLI declined by 13%. Larger-bodied, shallow-distributed, slow-growing species and those with range boundaries within the region are more likely to have worsening status in the Northeast Atlantic. Conversely, long- established, severe threat levels obscure any potential relationships between species’ traits and the likelihood of worsening IUCN status in the Mediterranean Sea. These regional RLIs provide the frst widespread evidence for increasing trends in regional shark and ray extinction risk and underscore that efective fsheries management is necessary to recover the ecosystem function of these predators.

Overfshing is the most imminent threat to many marine ­organisms1. Governments need repeated comprehen- sive assessments of extinction risk to efectively monitor the status of marine biodiversity­ 2 and track progress towards global biodiversity and sustainable development targets­ 3 if they are to halt declines, prevent more local , and recover species. Te Red List Index (RLI) tracks the changing extinction risk of groups of species based on status changes recorded on the International Union for Conservation of Nature Red List of Treatened Species­ 4 (hereafer ‘IUCN Red List’). Te RLI includes species listed under six categories, in ascending order of threat: Least Concern, Near Treatened, Vulnerable, Endangered, , and Extinct, but excludes the Data Defcient category­ 4. Tus far, the RLI has mostly been applied to terrestrial species, including birds, mammals, amphibians, and cycads­ 5–8. Our only understanding of changing marine extinction risk from the RLI so far comes from its application to stony corals, which reveals the threat of climate change to a key group of foundation species in the tropical ­oceans9. Tere remains a pressing need to develop an extinction risk trajectory representative of widely distributed marine fshes that are primarily threatened by overexploitation to better-understand the efects of this more immediate threat. Te RLI is eventually intended for global-level application, but like the Red List Assessments themselves, it is also informative when applied at regional and national scales­ 10 or decomposed by biome, habitat, conserva- tion profle, or international treaty­ 5. Here we focus on a regional Red List assessment because these fner-scale analyses better-connect species status and trajectory to local and regional variation in threats and conservation management across socio-political and economic ­regimes11,12. We focus on the sharks, rays, and ghost sharks (Class , herein ‘sharks and rays’) in the Northeast Atlantic Ocean and Mediterranean Sea for four reasons: (1) sharks and rays have the greatest percentage of ‘threatened’ species (i.e. Vulnerable, Endangered, or Critically Endangered) of any taxonomic Class of marine ­organisms13, with numerous populations worldwide already locally or regionally extinct due to ­overfshing1,14,15, including many from the Northeast Atlantic and Mediterranean Sea­ 16–18; (2) the status of sharks and rays in this region has been comprehensively assessed twice:

Earth to Ocean Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada. *email: [email protected]

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in 2003/2005 and in 2015­ 19–21; (3) the Northeast Atlantic and Mediterranean Sea may be a ‘canary-in-the-coal mine’ for collapse and recovery of fsh populations because of the combination of a long history of ­exploitation22, high scientifc capacity­ 17, substantial modern fshing efort­ 23, and divergent patterns of fsheries development and management­ 24; and (4) extinction risk categorisations have already been predicted for the Data Defcient species in these regions in previous research­ 25, presenting the opportunity to include these Data Defcient species in the RLI as well. One of the key challenges for the development of a taxonomically representative indicator is the high number of Data Defcient species listed, which until now have been excluded from trajectories of extinction risk even though some of them are predicted to be at ­risk25. Here, we provide a regional synthesis of the changing extinction risk for sharks and rays in the Northeast Atlantic and Mediterranean Sea (the RLI). We retrospectively assign IUCN categorisations to each species for the year 1980 through a critical review of historical fshing patterns and scientifc ­literature4,7,26. In our previously published research we predicted the IUCN categorisations of all Data Defcient species in 2015 (n = 21 North- east Atlantic, n = 12 Mediterranean)25, which we now incorporate into the RLIs alongside the IUCN-assessed categorisations (n = 98 + 21 = 119 Northeast Atlantic, n = 60 + 12 = 72 Mediterranean). We disaggregate the RLIs by primary habitat, then further explore the biological and ecological traits that are related to extinction risk. We build on the knowledge that sharks and rays with slower life histories (i.e. slower growth and population turnover rates­ 27–29) and shallower depth distributions (i.e. higher exposure to fshing activity due to limited depth refuge­ 30) are more likely to be categorised as threatened on the IUCN Red List­ 25,30 by exploring the likelihood of shark and ray Red List status worsening between assessment years based on these biological and ecological traits. Results and discussion Changes in extinction risk from 1980 to 2015. We compiled the results from the frst (2003 Mediterra- nean ­Sea19, 2005 Northeast Atlantic­ 20) and second (2015­ 18,21) regional IUCN Red List assessments of sharks and rays, then ‘backcast’ (i.e., retrospectively assigned an IUCN status) to 1980 through a critical review of historical fshing patterns and scientifc ­literature4,7,26 (see Methods for further detail and Supplementary Information for species-specifc backcasting justifcations). We fnd that sharks and rays in the Northeast Atlantic and Mediterranean Sea faced elevated levels of extinc- tion risk by 1980 and since then their status has steadily worsened (Fig. 1a). Te RLI is scaled from zero to one, where zero means all species are Extinct and one means all species are Least Concern­ 4. In the Northeast Atlan- tic the shark and ray RLI declined from a backcast value of 0.80 in 1980 to 0.74 in 2005 and further to 0.72 in 2015 (8% decline in RLI over 35 years; Fig. 1a). To represent the potential range of index values from the group assessed, we generated a confdence interval by bootstrapping (sampling with replacement) the 1980 statuses­ 31 (upper and lower confdence interval 0.85–0.75). Te change in Northeast Atlantic shark and ray status equates to an average rate of decline of 0.2% year­ -1. Te backcast Mediterranean Sea start-point was lower by 1980 than the 2015 Northeast Atlantic end-point, refecting greater Mediterranean extinction risk. Te Mediterranean RLI declined from a backcast value of 0.67 in 1980 (upper and lower confdence interval 0.74–0.61) to 0.59 in 2003, then to 0.54 in 2015 (13% decline in RLI over 35 years; Fig. 1a). In this region, the average rate of decline was 0.4% ­year−1, declining from 0.3% year­ −1 (1980–2003) to 0.4% year­ −1 (2003–2015). Between 1980 and 2015, the percentage of shark and ray species listed as threatened increased by 12% in the Northeast Atlantic (Fig. 1b) and 18% in the Mediterranean Sea (Fig. 1c). Almost one-third (29%, n = 35 of 119) of Northeast Atlantic sharks and rays were backcast into threatened categories in 1980 and this fraction rose to under two-ffhs (39%, 46) by 2005­ 20 and subsequently to over two-ffhs (41%, 49) by 2015­ 25 (Fig. 1b). In the Mediterranean Sea, almost half (47%, 34 of 72) of shark and ray species were backcast as threatened in 1980, and this fraction increased to over three-ffhs (61%, 44)19 by 2003 and further to nearly two-thirds (65%, 47) in 2015­ 25. Te divergence in extinction risk between ocean basins is apparent in the greatest percentage of Northeast Atlantic species listings being Least Concern (57%, n = 68 in 1980 and 45%, n = 54 in 2015; Fig. 1b). Conversely, while 32% (n = 23, the greatest percentage) of Mediterranean species listings were historically Least Concern in 1980, in 2015, the same percentage (32%, n = 23, the greatest percentage) are Critically Endangered. When calculating the RLI, the high weighting given to Critically made them a key driver of the lower RLI value in the Mediterranean Sea (Fig. 1c; see Methods for category weights). Te increasing extinction risk of Northeast Atlantic and Mediterranean sharks and rays is greater than any globally assessed vertebrate group on the RLI (Fig. 1a). Further, this risk is increasing faster than for other vertebrate lineages on the RLI: 7–9 times faster than global birds (1% decline in RLI over 26 years), 3–5 times faster than mammals (1% decline in RLI over 13 years), and 2–3 times faster than amphibians (4% decline in RLI over 26 years; Fig. 1a). Northeast Atlantic and Mediterranean sharks and rays are not declining as rapidly as the globally assessed Wedgefshes and Giant Guitarfshes (Family Rhinidae: 46% decline in RLI over 40 years)26 or pelagic (oceanic) sharks and rays (30% decline in RLI over 38 years)32. To put the high level of threat in context, there are as many threatened sharks and rays in Europe as there are threatened birds, but the threat level is nearly six times greater by percentage (41%, n = 56 of 136 sharks and rays threatened versus 7%, n = 56 of 792 birds threatened and ­Extinct33). Between 1994 and 2004, European birds were declining at three-quarters of the rate (2% decline in RLI over 10 years) of Northeast Atlantic sharks and rays and half the rate of Mediterranean sharks and ­rays34 (Fig. 1a). Decades of intense conservation efort has successfully reduced global bird declines­ 13 and averted ­extinctions35 maintaining them as the least threatened Class assessed on the global ­RLI5. By comparison, quotas in the Northeast ­Atlantic17 and a 1000 m depth limit for trawl and dredge fsheries in the Mediterranean Sea­ 36 were implemented only very recently in the early-2000s.

Disaggregating the Red List Index by primary habitat. Overfshing is the major threat identifed in the IUCN Red List Assessments facing all Northeast Atlantic and Mediterranean sharks and rays and in essence,

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Figure 1. Worsening status of Northeast Atlantic Ocean and Mediterranean Sea sharks and rays from 1980 to 2015. (a) Regional RLIs for sharks and rays in the Northeast Atlantic (n = 119; blue line) and Mediterranean Sea (n = 72; purple line), for birds in Europe (n = ­52234), and global RLIs for hard corals (n = ­7049), birds (n = ~ ­98396), mammals (n = ­46537), amphibians (n = ~ ­44156), and cycads (n = ­3038). Errors bars show the plausible range for each index value. Te stand-alone point for global sharks and rays indicates the 2006 starting point for the global shark and ray RLI­ 30. A RLI value of 1 represents a group of entirely Least Concern species while a value of 0 represents an entirely Extinct group. (b) Change in IUCN Red List status of Northeast Atlantic sharks and rays between 1980 and 2015 (LC: Least Concern, NT: Near Treatened, VU: Vulnerable, EN: Endangered, CR: Critically Endangered). (c) Change in IUCN Red List status of Mediterranean sharks and rays from 1980 to 2015. Colour gradients indicate changing species categorisations between IUCN assessments. Silhouette images were downloaded from phylopic.org and for the bird image specifcally we credit Jean- Raphaël Guillaumin and T. Michael ­Keesey©.

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Figure 2. Disaggregating the Red List Index reveals the most at-risk ocean habitats. Red List Indices for deepwater sharks and rays (Northeast Atlantic: n = 53 [circles], Mediterranean Sea: n = 13 [squares]), coastal and species (Northeast Atlantic: n = 36, Mediterranean Sea: n = 37), and pelagic species (Northeast Atlantic: n = 9, Mediterranean Sea: n = 10). Light grey lines indicate the regional RLIs for all of these species together (Northeast Atlantic: n = 98, Mediterranean Sea: n = 60). Confdence intervals represent the range of possible index values. A RLI value of 1 represents a group of entirely Least Concern species while a value of 0 represents an entirely Extinct group.

these RLIs provide a frst comprehensive evaluation of the efect of fshing pressure on marine biodiversity. When the RLIs are partitioned by primary habitat, deepwater species had the lowest-risk RLIs, with the rate of decline slowing by 50% since the early-2000s (Fig. 2, Table 1). Tis could be a refection of the expansion of deepwater fshing activity in the late 1980s to early 1990s alongside technological advancement­ 37, followed by a reduction in efort in the early-2000s owing to rising fuel costs­ 38 and the recent catch prohibitions for deepwater sharks­ 17, which was the partial basis of our backcasting decisions. Pelagic species face the highest extinction risk, followed closely by coastal species, although the decline rates are fairly similar for each (Fig. 2, Table 1). Globally, pelagic sharks and rays declined from a backcast RLI value of 0.86 in 1980 to 0.56 in 2018 (n = 31)32, yet Northeast Atlantic and Mediterranean sharks and rays face a higher risk of extinction than the global aver- age. However, the global rate of decline for pelagic sharks and rays is approximately twice that of this regional analysis, with an average rate of decline of 8% year­ −1,32. While the decline in coastal species was consistent throughout the study, pelagic species have declined slightly faster since the early-2000s (Fig. 2, Table 1). Tese increasing decline rates could be indicative of the need for greater international cooperation between managing bodies for these highly migratory species­ 39,40. All three habitat-based groupings reveal higher rates of decline in the Mediterranean Sea than the Northeast Atlantic. We removed the originally Data Defcient species from the disaggregated RLIs, therefore, these trends were not afected by the use of size and depth to predict the statuses of those species (n = 21 Northeast Atlantic, n = 12 Mediterranean).

Species’ status changes underlying the Red List Index trajectory. Two-thirds of Northeast Atlan- tic sharks and rays remained in the same IUCN category between 1980 and 2015 (63%, n = 75), while over half of all Mediterranean species’ statuses worsened during this time (44%, n = 32 remained in the same category in the Mediterranean Sea). In the Northeast Atlantic, 29% (n = 35) of species worsened by one IUCN category between the backcast 1980 assessment and 2005 (Fig. 1b) and 13% (n = 15) worsened by one category between 2005 and 2015 (Figs. 1b, Fig. 3a + b). Overall, 37% (n = 44) of Northeast Atlantic species’ statuses worsened between 1980 and 2015, of which 32% (n = 38) worsened by one category and 5% (n = 6) worsened by two cat- egories, e.g., Roughtail Stingray Dasyatis centroura, Smalltooth Sand Tiger Odontaspis ferox, Great Hammer- head Sphyrna mokorran, and Smooth Hammerhead Sphyrna zygaena (Fig. 1b). In the Mediterranean Sea, 42% (n = 30) of species worsened by one category between 1980 and 2003 (Fig. 1c), whereas between 2003 and 2015, 19% (n = 14) of species worsened by one category and 4% (n = 3) worsened by two categories from Vulnerable to Critically Endangered, e.g., Gulper Shark Centrophorus granulosus, Blue Shark Prionace glauca, and Smooth Hammerhead (Figs. 1c, and 3a + c). Overall, 56% (n = 40) of Mediterranean species’ statuses worsened between 1980 and 2015: 44% (n = 32) of species worsened by one category, 8% (n = 6) by two categories, e.g., Bignose Shark Carcharhinus altimus, Copper Shark Carcharhinus brachyurus, Dusky Shark Carcharhinus obscurus, and Sandy Skate Leucoraja circularis (Fig. 1c). Further, three species worsened by three categories from Near Treat- ened to Critically Endangered: Gulper Shark, Blue Shark, and Smooth Hammerhead (Fig. 1c). All species with worsening status between 1980 and 2015 have either one or a combination of (1) large body size (> 200 cm total length or disc width), (2) shallow depth distribution (upper depth limit < 500 m), (3) slow life history (generation

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Decline rate (% ­year−1) 1980–2003/5 Average decline rate (% ­year−1) Region Scope N Year RLI 2003/5-2015 1980–2015 Lower bound Upper bound 1980 0.80 0.75 0.85 0.2 All species 119 2005 0.74 0.2 0.69 0.79 2015 0.72 0.2 0.66 0.77 1980 0.92 0.86 0.97 0.2 Deep 62 2005 0.88 0.1 0.82 0.93 2015 0.87 0.1 0.81 0.93 Northeast Atlantic 1980 0.70 0.61 0.78 0.4 Coast 46 2005 0.61 0.4 0.53 0.69 2015 0.57 0.4 0.49 0.66 1980 0.60 0.45 0.77 0.3 Pelagic 12 2005 0.53 0.4 0.37 0.70 2015 0.48 0.5 0.33 0.65 1980 0.68 0.60 0.74 0.4 All species 72 2003 0.59 0.4 0.53 0.66 2015 0.54 0.4 0.46 0.61 1980 0.89 0.79 0.97 0.6 Deep 14 2003 0.76 0.5 0.66 0.86 2015 0.73 0.3 0.59 0.84 Mediterranean Sea 1980 0.64 0.55 0.73 0.3 Coast 49 2003 0.56 0.3 0.49 0.65 2015 0.51 0.3 0.44 0.60 1980 0.54 0.42 0.68 0.2 Pelagic 10 2003 0.50 0.5 0.38 0.64 2015 0.38 1 0.26 0.54

Table 1. Red List Index values for Northeast Atlantic and Mediterranean Sea sharks and rays between 1980 and 2015. Decline rates are calculated as the annual average between each assessment period, then the overall average taken from both periods.

length > 10 years), or (4) have a range boundary within this region (see Supplementary Fig. S2 and Supplemen- tary spreadsheet). For example, the Mediterranean Sea constitutes the northern limit for Bignose Shark, Copper Shark, Dusky Shark, and Smooth Hammerhead, and Europe is the fringe of the biogeographic distribution of at least seven warmer-water species (e.g. Roughtail Stingray, Smalltooth Sand Tiger, and Great Hammerhead). Species’ sensitivity to both overfshing and climate change is higher at their range ­boundaries41,42, which may explain the greater deterioration of these species’ statuses (Fig. 1b + c). Although there were six improvements in species status in the Northeast Atlantic and four in the Medi- terranean Sea, these changes are not refected in the RLI slopes because they are ‘non-genuine’4. Te IUCN defnes ‘genuine’ status change as actual change in, e.g., population size between Red List assessments, whereas ‘non-genuine’ changes could be from, e.g., new knowledge or taxonomic changes. ‘Non-genuine’ changes are therefore backcast to retrospectively refect new knowledge accordingly (see Methods section). For each of the ten improvements, new knowledge revealed the species to be better-of than assessors originally thought in the early-2000s. For example, the incorporation of improved understanding of density-dependent ofspring survival into the Northeast Atlantic stock assessment for Spiny Dogfsh (Squalus acanthias)43 resulted in a lower popula- tion reduction estimate and a ‘non-genuine’ change in status from Critically Endangered to Endangered. While these improvements were not refected in the RLI slopes due to retrospective correction of their 2005 status, they did contribute to the overall RLI values. Although these changes did not result from conservation eforts, they are still improvements of scientifc knowledge, which supports more accurate species assessment.

Slow life histories make sharks and rays susceptible to status deterioration. Tere is strong consistency in the geographic and biological patterning of shark and ray extinction ­risk27–29. We have previously shown that threatened shark and ray species tend to have slower life histories than non-threatened species (Least Concern and Near Treatened), demonstrated by the relationship between large body size and the likelihood of a shark or ray being listed in a threatened IUCN category­ 25,30 (Fig. 4a + b, Supplementary Fig. S1, Supplemen- tary Table S5). Here, we extend this ‘static’ trait-status pattern to show that Northeast Atlantic sharks and rays with deteriorating status tend to have slower life histories than species that did not change status between IUCN assessments, although the relationship is weaker for status-change than for static-status (Fig. 4a vs. c, Supple- mentary Fig. S1, Supplementary Table S1, S2). Te relationship between size and changing status is insignifcant in the Mediterranean Sea (Fig. 4d, Supplementary Table S1). Te intercept-only model ft best, indicating that

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Figure 3. Shark and ray species with worsening status in the Northeast Atlantic Ocean and Mediterranean Sea between 2003/5 and 2015. (a) Percentage of sharks and rays in the Northeast Atlantic and Mediterranean Sea with worsening versus static IUCN status between IUCN Red List assessments (Northeast Atlantic 2005–2015, Mediterranean Sea 2003–2015). (b) Shark and ray species with worsening status in the Northeast Atlantic between 2005 and 2015 and (c) between 2003 and 2015 in the Mediterranean Sea (LC: Least Concern, NT: Near Treatened, VU: Vulnerable, EN: Endangered, CR: Critically Endangered). Bold species names indicate a status change by two IUCN categories between assessments. Italicised species names indicate those for which IUCN status was predicted in previous ­research25. Line thickness (range 1–8) and point size (range 1–10) signifes number of species, as do numbers over each point and next to arrows. Species illustrations by Marc Dando­ ©.

size and depth do not explain changing status of Mediterranean sharks and rays. Tis is in part because there are fewer true deepwater shark and ray species in the region (Fig. 4d, Supplementary Table S1). We have also shown previously that threatened shark and ray species tend to have shallower depth distri- butions than non-threatened species, which we interpret as the efect of refuge from fshing activity at greater ­depth25,30 (Fig. 4a + b, Supplementary Fig. S1, Supplementary Table S1). Shallower depth also correlates with a likelihood of worsening status in the Northeast Atlantic, for which the top model included both size and depth (Fig. 4c, Supplementary Fig. S1, Supplementary Table S1). Tese fndings were not changed by the inclusion of previously Data Defcient species in our models for which IUCN status was predicted­ 25, as the model hierarchy is the same when these species are removed from the analysis (Supplementary Table S1, S3). Further, these pat- terns are the same when taxonomic family is included as a random efect, though the inclusion of taxonomic family weakened the models in general (Supplementary Tables S1, S3, S4). Te deepening of fshing activity in the early-1990s—particularly in the Northeast Atlantic—has increased the extinction risk of deepwater species over the past 40 ­years44. However, that is not to say that deepwater Northeast Atlantic sharks and rays are more at-risk than shallower species. Rather, shallower species were already at high

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risk prior to the fshing down of the deepwater species, which reached a similar level of risk during the 1990s. We recognise the recursive nature of this inference, given the prior knowledge of depth ofering refuge for sharks and ­rays25,30 and the basis of our backcasting decisions partly being the expansion of fsheries into deeper ­waters37. In the present study, the implicit assumption when backcasting species’ IUCN status is that fshing efort and spatial overlap of fsheries with species’ ranges are highly correlated with the declining abundance of sharks and rays in the Northeast Atlantic and Mediterranean Sea. Tis is a fundamental assumption of ecological risk assessments. However, the abundance data required to test this assumption are not yet available for sharks and rays in these regions. In future, it would be helpful to test the rigidity of this assumption when these data are available. Tis would require extensive exploration of the spatial patterning of both fsheries and species, perhaps best undertaken by scientifc councils such as the International Council for the Exploration of the Sea’s Working Group for Elasmobranch Fishes. Te consideration of changing-status alone overlooks any species that remained in the Endangered and Critically Endangered categories from 1980–2015 – most notably in the Mediterranean Sea (15%, n = 18 of 119 Northeast Atlantic: six remained Endangered and 12 remained Critically Endangered; and 25%, n = 18 of 72 Mediterranean: fve remained Endangered and 13 remained Critically Endangered, from 1980 to 2015). Tis substantial percentage of species are all large-bodied and have shallow depth distributions and hence their inertia on the RLI (because they are already nearly as high-risk as can be categorised) washes out the correlation between these traits and changing status, particularly within the Mediterranean data. In fact, once these spe- cies are removed from the analysis the probability of sharks and rays having a worsening status based on their maximum size and median depth is very similar to the probability of being threatened (Fig. 4e + f compared with Fig. 4a + b, Supplementary Fig. S1, Supplementary Tables S2, S4, S5). Te strength of the models increases consid- erably when these species are removed and changes the model hierarchy so that both size and depth are related to changing status in both regions, whether taxonomic family is included as a random efect or not (Supplementary Tables S2, S4). Tis highlights an important consideration: the RLI does not refect ongoing species population decline unless the decline is sufcient to cross IUCN category thresholds­ 45. Hence, these trajectories are likely a conservative representation of true population decline levels in the Northeast Atlantic and Mediterranean Sea. Conclusions Investing in management to secure a future for overexploited marine species. Sustainable exploitation underpins food security and the well-being of ­humanity46. Many fsh stocks have collapsed and while strict management measures have recently reversed some declines in the Northeast Atlantic, insufcient action has been taken to halt or reverse declines in the Mediterranean ­Sea24. Tere are profound and long-recog- nised diferences between Northeast Atlantic and Mediterranean fsheries ­management24,47. Although numerous solutions to the plight of Mediterranean fsheries have been suggested, few have been efectively implemented for the beneft of sharks and ­rays47–49. Both regions have been heavily fshed for ­centuries22, and consequent shif- ing baselines undermine true levels of decline­ 50. Te RLIs presented do not convey the considerable degree of population decline and collapse that occurred in the Northeast Atlantic and Mediterranean Sea prior to 1980 as a direct result of ­overfshing2,23,51, nor do the GLMs for changing status (Fig. 4). Drastic improvement of shark- and ray-focused fsheries management is required to deliver on marine biodiversity goals by halting declines and preventing regional species extinctions, particularly in the Mediterranean ­Sea24,49,52. While countries have obligations to improve the status of sharks and rays, improvements in the management of these sensitive species may also yield long-term benefts of more sustainable fsheries for other species, and indeed for human well- being and livelihoods all around the Mediterranean coast too. Cooperation and higher prioritisation are generally needed to improve the status of sharks­ 53–55. Just as the poor status of birds led to the creation of the European ‘Birds Directive’ and extensive improvements in agriculture­ 56, the status of sharks and rays reported here would justify the creation of a European ‘Sharks and Rays Directive’ to transform fsheries. Although the European Union’s fsheries management reforms have reversed stock declines of some commercially important teleost species in the Northeast ­Atlantic24,52, we raise fve points of concern about fsheries management in the Northeast Atlantic and Mediterranean Sea. First, shark and ray management was only recently implemented in the Northeast Atlantic, while the Mediterranean Sea has essen- tially been overlooked­ 24,52,57. Second, Northeast Atlantic shark and ray protections were implemented only afer population collapse, thus recovery could take ­decades58. Tird, frequent reports of captured protected species on social media reveal that while catching some species is prohibited, there is ofen limited awareness among fshers of these protections, especially in the Mediterranean ­Sea59. Fourth, the one measure in place to protect Mediterranean sharks and rays is a ban on fshing below 1000 m ­depth36, but we show here (based on the narrow depth quartiles for Mediterranean species in Fig. 4b + d + f) that this measure is potentially benefting only a small minority of species at the deepest end of their depth ranges. Finally, there are few resources or funding programs that we are aware of that implement existing protections, with the conservation planning and implementation slack being largely picked-up by Non-Governmental Organisations­ 16. International cooperation between fsheries managers is essential for the beneft of those species that regularly migrate signifcantly outside the geographic extent considered in the present study (e.g. those listed in Appen- dix I and II of the Convention on the Conservation of Migratory Species of Wild ­ 60), as these species are inevitably exploited in waters outside of the jurisdiction of the European ­Union53–55. Indeed, when these migratory species are removed from the RLIs (17%, n = 20 from 119 Northeast Atlantic and 22%, n = 16 from 72 Mediterranean species), both of the index values improve overall by ~ 5% due to the relatively high extinction risk faced by these migratory and range-boundary species (Supplementary Fig. S2).

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The Northeast Atlantic and Mediterranean Sea could be a ‘canary‑in‑the‑coal mine’. Te situ- ation in the Northeast Atlantic and Mediterranean Sea may refect levels of extinction risk in other regions with equivalent fshing levels and management capacity. For example, aside from seasonal closures, there is rela- tively little regulation of fsheries in the Arabian Seas and adjacent waters and consequently 51% (n = 78 of 153) of sharks and rays are threatened ­regionally61, which is close to the status in the Mediterranean Sea. Without monitoring and periodic evaluation, the local extinction of the more sensitive species may be overlooked, as has already happened frequently, such as for the Angel Shark (Squatina squatina), Bramble Shark (

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◂Figure 4. Efect of maximum body size and median depth on Northeast Atlantic Ocean and Mediterranean Sea shark and ray status. Te probability that a shark or ray species will be threatened (1: Vulnerable, Endangered, Critically Endangered) or non-threatened (0: Least Concern, Near Treatened) due to the combination of intrinsic biological sensitivity (maximum size, cm total length of sharks, skates, and ghost sharks, or wing span of rays) and exposure to fsheries (median depth, m) in the Northeast Atlantic (a) and Mediterranean Sea (b). Te probability that a shark or ray’s IUCN status will worsen (1) or stay the same (0) according to the same traits (Northeast Atlantic: c, Mediterranean Sea: d) and the same test afer removing species that remained in the Endangered and Critically Endangered categories from 1980–2015 (Northeast Atlantic: e, Mediterranean Sea: f). Models are based on 118 Northeast Atlantic and 71 Mediterranean shark and ray species, excluding the outlier Basking Shark (panels a–d), and 100 and 53 species, respectively (panels e + f). Lines are the best fts from Generalised Linear Models with IUCN status (a,b) and status change (c–f) as the response and maximum size and median depth as the fxed efects (see Supplementary Tables S1, S4, S5). Lines were calculated for the lower (shallow, lightest blue), median, and upper (deep, darkest blue) depth quartiles of each species set. Vertical pink bars represent species with threatened (1; a,b) or worsening (1; c–f) status and green bars non-threatened (0; a,b) or non-changing (0; c–f) status positioned according to their maximum size.

brucus), Common Skate complex (Dipturus batis and D. intermedia), and other large ­skates51, 62–64. Stock assess- ments (i.e. species-specifc population trend data) of marine fshes—which are largely unavailable for sharks and rays—are typically completed on a smaller scale than IUCN regional or global analyses of extinction risk, although the IUCN Guidelines advise assessors on the use of such data to ensure appropriate proportional rep- resentation of stocks within assessment ­regions65. Te RLI currently provides the most efective, widely-accepted means of monitoring changing extinction risk, particularly for data-poor ­groups66,67. Our methods are intended for application to the forthcoming global shark and ray RLI, which will eventually reveal how representative the Northeast Atlantic and Mediterranean Sea are of global shark and ray status. Indeed, we know already that the 2014 starting point of the global shark and ray RLI is in a position of greater extinction risk than the lat- est global Red List assessments for birds, mammals, and corals, but still lower-risk than this regional Red List ­assessment30 (Fig. 1a). Our methods are applicable to any species group assessed by the IUCN more than once, can be extrapolated to any geographic scale, and the implications outlined here are relevant to any species group that is also threatened predominantly by overexploitation.

Enhancing progress‑tracking towards future biodiversity targets. Te exclusion of Data Defcient species from risk indicators undermines global-level reporting on progress towards biodiversity and sustain- ability ­targets68. Using biological and ecological trait data to incorporate Data Defcient species into extinction risk tracking is currently the most cost-efective, expeditious method for understanding aggregate extinction risk and informing appropriately and efciently directed species ­conservation69. Tere was minimal efect on the Northeast Atlantic and Mediterranean RLIs from adding predicted species statuses­ 25, refecting a broad similar- ity in the biological and ecological trait distributions of the Data Defcient and data-sufcient sharks and rays (Fig. 5). We caution that there are numerous reasons not to expect this similarity in less well-studied regions, where even the most sensitive species may not yet be taxonomically described or assessed but are potentially at risk of ­extinction26,70. Te Convention on Biological Diversity 2020 Aichi targets and the United Nations 2020 Sustainable Devel- opment Goals have been missed for Northeast Atlantic and Mediterranean sharks and rays. Tere may only be a decade or so to realistically halt and reverse global biodiversity loss before the updated Kunming Target deadline­ 71. Here, we demonstrate that the Red List Index can incorporate the status predicted for data-poor spe- cies or species-groups and the inclusion of these species enables the most complete progress-reporting possible towards imminent deadlines. Methods Collation of regional IUCN Red List assessments. We consider a total of 127 unique species, includ- ing 119 Northeast Atlantic and 72 Mediterranean, with 57 species spanning both regions (hence, 62 exclusively Northeast Atlantic and 15 exclusively Mediterranean). Species spanning both regions are assigned a separate category for each region, many of which are the same. Of the assessed species there are 49 skates and rays (Order Rajiformes), 70 sharks (Order Carcharhiniformes, Hexanchiformes, Lamniformes, , Squatini- formes), and eight ghost sharks (Order Chimaeriformes). Tis list does not include two species assessed by the IUCN as they are no longer considered breeding residents (Tiger Shark Galeocerdo cuvier and Marbled Stingray Dasyatis marmorata). Species not breeding in the region are considered ‘vagrant’ according to IUCN ­terminology65. All species included in the analysis were agreed by IUCN Red List assessors to be valid regionally at the 2015 workshop. We classify species according to their primary habitat in accordance with IUCN Red List assessment, allocating those species that span multiple habitats according to the habitat in which they spend the majority of their life cycle. Coastal/continental shelf species are mainly demersal bottom-dwelling (< 200 m depth), with deepwater species predominantly deeper than the continental shelf (≥ 200 m depth), and pelagic species mostly in open, ofshore ­water30. Te Northeast Atlantic and Mediterranean Sea were assessed by the IUCN Shark Specialist Group both in 2003/200519,20 and 2015­ 25 and the Red List assessments from 2015 were merged to present a regional IUCN Red List assessment to the European ­Union21. All IUCN Red List assessments from 2003, 2005, and 2015 were com- pleted according to the IUCN Categories and Criteria, version 3.145. Te 2003/2005 assessments were completed using the frst edition of the version 3.1 criteria­ 72 and the 2015 assessments using the second edition­ 45. Te same

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Figure 5. Northeast Atlantic Ocean and Mediterranean Sea Data Defcient sharks and rays have similar trait distribution to data-sufcient species. Relative distribution of IUCN status for n = 119 Northeast Atlantic and n = 72 Mediterranean shark and ray species based on maximum size (cm, total length for sharks, skates, ghost sharks or wingspan for rays) and median depth (m; as a measure of accessibility to fshing vessels). Circular coloured points represent species assessed as data-sufcient by the IUCN in 2015, while Data Defcient species are marked by X symbols. Te Y axis is inverted to represent ocean depth. Point colour corresponds to IUCN status: Critically Endangered—red, Endangered—orange, Vulnerable—yellow, Near Treatened—light green, Least Concern—darker green, and Data Defcient—dark grey.

Red List assessment system is maintained in both editions, the IUCN updated the document in order to adapt and maintain its usefulness as a conservation tool alongside ongoing technological advances in data analysis­ 45. Te IUCN published an overall status designation for each species when reporting to the European ­Union21 and did not report diferences between the Northeast Atlantic and Mediterranean Sea sub-regions. To avoid masking status changes for higher-risk species in the Mediterranean Sea, we went back to the separate sub-region status evaluations completed in the 2014 workshop, rather than the published, combined IUCN Red List (see Supple- mentary data for the originally reported merged categorisations and all alternative versions of categorisations). We consider only the fve main extant (‘data-sufcient’) IUCN categories in the present study by replacing all Data Defcient listings with the predicted categorisations from previous research­ 25. We therefore consider both assessed and predicted listings of Least Concern, Near Treatened, and the three ‘threatened’ categories (in ascending order of threat): Vulnerable, Endangered, and Critically Endangered­ 65. Te predicted statuses from previous research for all Data Defcient species in the Northeast Atlantic and Mediterranean Sea are considered among IUCN-assessed statuses throughout the present study without ­diferentiation25, i.e. the predicted listings have the same infuence on the RLI value as the assessed listings and there is no weighting or subjective quality assigned to the predicted statuses. All data-sufcient Northeast Atlantic and Mediterranean sharks and rays were assessed by the IUCN based on population size, under the IUCN’s Criterion A. Criterion A is assigned based on thresholds of percentage population reduction over a three-generation period either ‘estimated’, ‘inferred’, or ‘suspected’ over the greater of ten years or three generation ­lengths65. Tese IUCN terms (listed in order of decreasing data-certainty) have specifc meaning when used in IUCN assessments, acting as sub-categories, and the same meaning is intended in the present study. Whereas estimated declines (and the status categorisation they inform) are typically based on landings and catch data, inferred or suspected declines require some assumption. Tese categorisations are typically inferred from similar, more data-rich species or either inferred or suspected from information such as geographic and depth range that can be used to discern the degree of overlap with fsheries. A ‘similar’ species would ideally be a congener of similar maximum body size, depth range, generation length, and with the same threats (e.g. Bigeye Tresher Shark Alopias superciliosus from Common Tresher Shark Alopias vulpinus, see spreadsheet in Supplementary Information). Te 2015 Red List reassessments were completed by multiple assessors, peer reviewed by two additional experts, then consistency checked by the Red List Authority to ensure utmost consistency of terminology and that a precautionary view of the evidence was applied across ­assessments73. Te variation in subjectivity between assessors in each assessment year is minimised through the application of the IUCN Red List ­Guidelines65, training materials, and guidance on what value system to use when assessing, i.e. precautionary instead of evidentiary. In the early-2000s, the ‘evidentiary approach’ to assessing was more common among fsheries scientists, whereas the ‘precautionary approach’ has been more strictly adopted since the reassessment began in 2014. Te evidentiary approach relies almost entirely upon available population data, whereas the precautionary approach encourages the use of all supporting informa- tion to determine extinction risk across the spectrum of certainty outlined above, even in the absence of actual population data, and encompassing a wider range of traditional and fshers’ ecological ­knowledge16,74–76. We do

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not account for the varying degrees of uncertainty statistically and instead treat all listing-certainty, including that of the predicted listings from previous ­research25, as equal in our statistical models. See Supplementary Data for the original IUCN status designations that were retained for analyses.

Backcast historical categorisations. For IUCN assessments, backcasting is the process of adjusting his- torical categorisations to refect new knowledge and was introduced to standardise the process of adding new species to the RLI as well as to retrospectively correct species status­ 4,7,26. Te basis for backcasting is the same as for writing ofcial IUCN Red List assessments: the pertinent available information is gathered and used to assign an historical extinction risk categorisation using a precautionary approach­ 4,7,26. For the present study, this included life history and ecology information from scientifc literature, fshing records, reports on trends in fshing efort, and the Red List assessments completed in the early-2000s and 2015­ 26,32. Te choice of a back- cast timeline is a trade-of between efect size (a longer timeline is likely to have a greater diference in status) against the decreasing availability of data (the further back in time we go, less data and knowledge are available). We chose to backcast status to 1980 due to (1) data availability; (2) fshing efort doubling in the Northeast Atlantic and Mediterranean Sea between 1950 and ­198023; and (3) deepwater fshing capacity expanding from a maximum depth of ~ 800 m to > 1000 ­m37 in the late-1980s to early-1990s. For most species, the available information allowed a degree of certainty in line with ‘inference’, as per the levels of IUCN-assessment cer- tainty outlined above. For example, the Common Skate complex (Dipturus batis and D. intermedius) is known to have been depleted by 1980 due to heavy fshing pressure because a publication in 1981 already warned of its near-extinction51. Tis species was therefore backcast from 2015 and 2005 statuses of Critically Endangered to have already been Critically Endangered in 1980. A similar situation was true for the Angel Shark (Squatina squatina)77,78. Further, all deepwater species with little or none of their depth range shallower than 800 m depth were inferred to be Least Concern in 1980 unless catch or landings data showed otherwise. Tis assumption was based on the refuge these species had at depth before deepwater fsheries expanded to depths > 1000 m in the early-1990s37, so the degree of certainty is in line with inference. Similarly, all species listed as Least Concern in the early-2000s and 2015 were assumed to have been Least Concern in 1980 as well, as the overall increasing regional fshing efort makes it unlikely that these species would have been higher-risk previously. A more com- plicated example is the Gulper Shark (Centrophorus granulosus) in the Mediterranean Sea, as follows: (1) at least half of this species’ depth range (100–1490 m) has overlapped with fshing activity since the 1950s; (2) it has a very long 20-year generation length and consequent slow population turnover; (3) it was listed as Vulnerable in 2003 afer deepwater fshing efort increased considerably in the 1990s and was therefore likely lower-risk prior to the 1990s; but (4) it is unlikely that this species was Least Concern in 1980 due to the combination of points (1) and (2). Hence, we backcast the 1980 status for Gulper Shark as Near Treatened. For all other species-specifc justifcations for backcasting of status and the supporting data and literature, please refer to the spreadsheet in the Supplementary Information. We note that the process of backcasting has few choices. For example, a spe- cies listed as Vulnerable in 2015 and Near Treatened in 2005 must have been either Near Treatened or Least Concern in 1980 based on our knowledge of fshing trends. To conservatively account for the uncertainty around the 1980 categorisations we used the ‘red’ package in R to calculate confdence intervals for the RLI values by bootstrapping 1000 iterations of each status ­assignment31. Te confdence intervals generated do not account for the uncertainty in assigned status of individual species, rather they show the range of possible values for the RLI of the species group as determined from the group as it was assessed. Terefore, the bootstrapping assumes that the status designations are representative of sharks and rays in the region. Te early-2000s Red List assessments were originally highly conservative because of the evidentiary mindset that was prevalent among fsheries scientists at the time. Since the early-2000s, knowledge of fsheries target and limit reference points has improved owing to empirical and simulations analyses of numerous teleost and elasmobranch ­populations24,79, as well as the precautionary approach being consistently adopted during the later Red List assessments. We therefore backcast several of the 2003/2005 statuses to be in-line with this new knowledge and the precautionary approach (see spreadsheet in Supplementary Information). For example, the Common Tresher Shark had originally been listed as Near Treatened in the Northeast Atlantic in 2005 using an evidentiary approach. Te 2015 status was decided as Endangered using the precautionary approach, which created an unrealistically steep decline from Near Treatened to Endangered over the ten years between 2005 and 2015. In this case, the 2005 status was backcast as Vulnerable based on new knowledge of the species’ general decline, particularly the fact that fshing efort across this species’ range doubled between 1950 and 1980 and was comparably stable between 2005 and 2015­ 23. Te majority of population decline was therefore likely to have occurred long before 2005 (see spreadsheet in Supplementary Information for justifcation of statuses altered from the early-2000s). We also conservatively backcast species that were listed as Data Defcient in 2003/2005 but became data- sufcient by 2015, as per the standard backcasting protocol adopted by the IUCN­ 4. Tese species were backcast under the same category as the 2015 IUCN Red List assessment unless evidence was available of ‘genuine’ improvement or deterioration in status of sufcient magnitude to cross IUCN category thresholds since the early-2000s4. Whereas a genuine species status improvement (not seen in this study) might result from suc- cessful conservation eforts, ‘non-genuine’ improvements that occurred between the early-2000s and 2015 were a result of, for example, gained knowledge that revealed the previous assessment to be overly evidentiary and insufciently ­precautionary80. Most category changes between IUCN assessments are non-genuine due to new information becoming available, hence, due to backcasting they are not refected in the RLI slope. Te same backcasting approach as outlined above was used in these instances (see spreadsheet in Supplementary Informa- tion for comparison of all original and backcast statuses).

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Calculating the extinction risk trajectory: the Red List Index. We calculated RLIs from the 119 Northeast Atlantic and 72 Mediterranean shark and ray Red List assessments from 2003/2005 and 2015, and the 1980 backcast. A RLI value is calculated for each assessment year based on the proportion of species listed in each IUCN Red List category. Te point of the RLI is to show the overall change in extinction risk over time (i.e. extinction risk trajectory) and it cannot be reliably interpreted otherwise, i.e. it does not convey the proportion of published listings in each category at any given time. For the calculation of each RLI value, the IUCN Red List categories are weighted such that the greater the threat category, the greater the weight: Least Concern = 0, Near Treatened = 1, Vulnerable = 2, Endangered = 3, Critically Endangered = 4, and (Regionally) Extinct (EX) = ­54 (there were no Regionally Extinct species to consider in the present study). Each category change between assessment years is equally weighted such that a status change from Least Concern to Near Treatened is equal to changing from Critically Endangered to Extinct in terms of its overall infuence on the RLI ­slope4. Te decline between categories is therefore linear and the decline rate of the index is dependent on the number of categories considered. Te RLI value of a particular year (t) is calculated by multiplying the sum of all species (s) in each IUCN category by the relevant category weight (W), then summing the product and dividing by the maximum 4 possible product (number of species: N, multiplied by the maximum category weight: WEX = 5) . Finally, this value is subtracted from one to give an index value between zero (all species are Extinct) and one (all species are Least Concern)4. Tis calculation is completed separately for each assessment year under consideration. Te RLI is represented by Eq. (1)4:

s Wc(t,s) RLIt = 1 − (1) WEX · N

Testing for a diferential efect of size and depth on worsening IUCN Red List status. We then tested whether changes in IUCN status were related to biological or ecological traits of assessed species, refect- ing the prior knowledge that intrinsic sensitivity to fshing pressure, combined with the degree of exposure to fshing activity, is functionally related to IUCN ­status25,30. We ran binomial Generalized Linear Models (GLMs) using the glm function in R version 3.5.281 with maximum size and median depth as fxed efects and IUCN status (non-threatened = 0, threatened = 1) or status change (no status change/improving status = 0, worsening status = 1) as the response. We also ran equivalent Generalized Linear Mixed-efects Models (GLMMs) with 82 binomial error and a logit link using the glmer function in the lme4 ­package , including taxonomic family as a random efect to account for phylogenetic ­covariation83,84. We also ran the models for each region (a) replac- ing the response variable with ‘2015 static IUCN status’ (n = 118 Northeast Atlantic and n = 71 Mediterranean species in both sets of models, excluding the outlier Basking Shark Cetorhinus maximus), and (b) excluding all species that remained in either the Endangered or Critically Endangered categories from 1980 to 2015 (n = 100 Northeast Atlantic and n = 53 Mediterranean species), for comparison. We modelled two biological and ecologi- cal traits (fxed efects) to discern difering threat levels between the Northeast Atlantic and Mediterranean Sea: maximum body size as a measure of intrinsic sensitivity and median depth as a measure of exposure to fshing activity. Te working model is represented by Eq. (2):

pi log − pi = β0 + βi,jXi,j + β X 1  i,k i,k (2) where the probability of a species (i) having ‘worsening IUCN status’ is assumed to be binomially distributed with a mean pi, where β0 is the coefcient estimate for the intercept, βi,j and βi,k are the ftted coefcients for maximum 83,84 size (j) and median depth (k), and Xi,j and Xi,k are the trait values of j and k for species i . We compiled all data from the regional IUCN Red List assessments completed in ­201518,21. We centred and scaled size and depth by two standard deviations­ 85 so that the efect size of these continuous variables was equivalent to a binary predic- tor, allowing us to directly compare them to the binary status change. Te probabilities used to plot the lines in Fig. 4 were extracted manually in R by exponentiating the log(probability) from Eq. (2) for each species. We used 86 the Akaike Information Criterion corrected for smaller sample sizes (AIC­ c) and ranked models according to their delta ­AIC87 (zero is the highest ranked model with any model two or fewer AIC units away from zero not signifcantly diferent from the best). To evaluate model ft, we used the MuMIn package version 1.43.1588 in R to calculate marginal and conditional R-squared values for the GLMMs and pseudo-R-squared values for the GLMs. We tested for collinearity between maximum body size and median depth by calculating the variance infation factor (vif) using the car package version 3.0-789 in R. Te values for both regions fell below three (both were close to one), which is typically used as an upper limit­ 90, indicating acceptably low collinearity for inclusion of both variables in the models. Data availability Te original data used in this manuscript are publicly available at iucnredlist.org. We have also provided a sum- mary spreadsheet of all of the data in the Supplementary Information.

Received: 10 October 2020; Accepted: 5 July 2021

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Acknowledgements We thank all members of the IUCN Species Survival Commission, in particular Craig Hilton-Taylor, Jean- Christophe Vié, Anna Nieto, and Caroline Pollock, and the IUCN SSC Shark Specialist Group and other experts who contributed to the data collation, assessment and review processes, especially workshop participants Alvaro Abella, Simona Clo, Manuel Dureuil, Jim Ellis, Edward Farrell, Francesco Ferretti, Sonja Fordham, Sarah Fowler, Ali Hood, Armelle Jung, Sophy McCully, Fabrizio Serena, David Sims, Alen Soldo, Matthias Stehmann, and

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Heike Zidowitz. Tis project was funded by the Shark Conservation Fund, a philanthropic collaborative pooling expertise and resources to meet the threats facing the world’s sharks and rays. We thank John Reynolds, Arne Mooers, Nathan Pacoureau, and all members of the Dulvy Lab and ­Earth2Ocean Lab for comment on drafs and statistical advice. We thank Marc Dando for the illustrations in Figure 3 and phylopic.org for the silhouettes in Figure 1 (for the bird silhouette specifcally, Jean-Raphaël Guillaumin and T. Michael Keesey). We thank the multiple anonymous reviewers of this manuscript for their constructive feedback. Author contributions Both authors are responsible for conceptualization, data curation (including completing Red List assessments), investigation, methodology and visualisation. R.H.L.W.: Formal analysis, Writing—Original draf. N.K.D.: Fund- ing acquisition, project administration, supervision, validation, writing—review & editing. Funding Te Shark Conservation Fund is a project of Rockefeller Philanthropy Advisors. Te European Red List of marine fshes was a project funded by the European Commission (Directorate General for the Environment under service contract number 070307/2011/607526/SER/B.3). Rachel Walls and Nicholas Dulvy were supported by a Natural Science and Engineering Research Council Discovery and Accelerator Award and Nicholas Dulvy was supported by the Canada Research Chairs Program. Rachel Walls was also supported by the Simon Fraser University Graduate Fellowship award program.

Competing interests Te authors declare no competing interests. Additional information Supplementary Information Te online version contains supplementary material available at https://​doi.​org/​ 10.​1038/​s41598-​021-​94632-4. Correspondence and requests for materials should be addressed to R.H.L.W. Reprints and permissions information is available at www.nature.com/reprints. Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional afliations. Open Access Tis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. Te images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/.

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